A combined α7 nicotinic acetylcholine receptor agonist and monoamine reuptake inhibitor, NS9775, represents a novel profile with potential benefits in emotional and cognitive disturbances

Neuropharmacology

Volumn 73, Issue , 2013, Pages 183-191

  Andreasen, Jesper T ^a   Redrobe, John P ^b   Nielsen, Elsebet Ø ^c   Christensen, Jeppe K ^c   Olsen, Gunnar M ^c   Peters, Dan ^d,e  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b H LUNDBECK A S   (Denmark)

^c NEUROSEARCH A S   (Denmark)

^d DanPET AB   (Sweden)

^e Aniona   (Denmark)

Author keywords

Anxiety; Behaviour; Cognition; Comorbidity; Depression; Mice; Monoamine reuptake inhibition; 7 nicotinic receptor agonism

Indexed keywords

3BETA (4 FLUOROPHENYL) 2BETA TROPANECARBOXYLIC ACID METHYL ESTER; 4 CHLORO N (3 QUINUCLIDINYL)BENZAMIDE; 6 (1 AZABICYCLO[2.2.2]OCT 2 EN 3 YL)NAPHTHALEN 2 OL HYDROCHLORIC ACID; ALPHA BUNGAROTOXIN; ALPHA1 NICOTINIC ACETYLCHOLINE RECEPTOR; ANTIDEPRESSANT AGENT; BUNGAROTOXIN RECEPTOR; BUNGAROTOXIN RECEPTOR AGONIST; DIZOCILPINE; DOPAMINE; METHYLPHENIDATE; MONOAMINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; NORADRENALIN; NS 9775; SCOPOLAMINE; SEROTONIN; TRANQUILIZER; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; ATTENTION DISTURBANCE; AVOIDANCE BEHAVIOR; BRAIN CORTEX; COGNITIVE DEFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE UPTAKE; DRUG ACTIVITY; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; EMOTIONAL DISORDER; EX VIVO STUDY; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; IC 50; IN VITRO STUDY; IN VIVO STUDY; LEARNING DISORDER; MALE; MAZE TEST; MEMORY DISORDER; MONOAMINERGIC SYSTEM; MOUSE; NONHUMAN; NORADRENALIN UPTAKE; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTONIN UPTAKE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TRANQUILIZING ACTIVITY; WORKING MEMORY;

ANXIETY; BEHAVIOUR; COGNITION; COMORBIDITY; DEPRESSION; MICE; MONOAMINE REUPTAKE INHIBITION; Α7 NICOTINIC RECEPTOR AGONISM;

AFFECTIVE SYMPTOMS; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN; BUNGAROTOXINS; COGNITION DISORDERS; DRUG EVALUATION, PRECLINICAL; FEMALE; MALE; MAZE LEARNING; MICE; NAPHTHALENES; NEUROTRANSMITTER UPTAKE INHIBITORS; NICOTINIC AGONISTS; PUNISHMENT; RADIOLIGAND ASSAY; TRITIUM;

EID: 84885091106     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.04.060     Document Type: Article

References (75)

1. Advokat, C., 2010. What are the cognitive effects of stimulant medications? Emphasis on adults with attention-deficit/hyperactivity disorder (ADHD). Neurosci. Biobehav. Rev. 34, 1256-1266.
2. Amado-Boccara, I., Gougoulis, N., Poirier Littre, M.F., Galinowski, A., Loo, H., 1995. Effects of antidepressants on cognitive functions: a review. Neurosci. Biobehav. Rev. 19, 479-493.
3. Andreasen, J.T., Andersen, K.K., Nielsen, E.O., Mathiasen, L., Mirza, N.R., 2006. Nicotine and clozapine selectively reverse a PCP-induced deficit of PPI in BALB/cByJ but not NMRI mice: comparison with risperidone. Behav. Brain Res. 167, 118-127.
4. Andreasen, J.T., Olsen, G.M., Wiborg, O., Redrobe, J.P., 2009a. Antidepressant-like effects of nicotinic acetylcholine receptor antagonists, but not agonists, in the mouse forced swim and mouse tail suspension tests. J. Psychopharmacol. 23, 797-804.
5. Andreasen, J.T., Nielsen, E.O., Redrobe, J.P., 2009b. Chronic oral nicotine increases brain [3H]epibatidine binding and responsiveness to antidepressant drugs, but not nicotine, in the mouse forced swim test. Psychopharmacology (Berl) 205, 517-528.
6. Andreasen, J.T., Redrobe, J.P., 2009. Nicotine, but not mecamylamine, enhances antidepressant-like effects of citalopram and reboxetine in the mouse forced swim and tail suspension tests. Behav. Brain Res. 197, 150-156.
7. Andreasen, J.T., Nielsen, E.O., Christensen, J.K., Olsen, G.M., Peters, D., Mirza, N.R., Redrobe, J.P., 2011. Subtype-selective nicotinic acetylcholine receptor agonists enhance the responsiveness to citalopram and reboxetine in the mouse forced swim test. J. Psychopharmacol. 25, 1347-1356.
8. Andreasen, J.T., Redrobe, J.P., Nielsen, E.O., 2012. Combined alpha7 nicotinic acetylcholine receptor agonism and partial serotonin transporter inhibition produce antidepressant-like effects in the mouse forced swim and tail suspension tests: a comparison of SSR180711 and PNU-282987. Pharmacol. Biochem. Behav. 100, 624-629.
9. Bertrand, D., 2005. The possible contribution of neuronal nicotinic acetylcholine receptors in depression. Dialogues Clin. Neurosci. 7, 207-216.
10. Biederman, J., Spencer, T., Wilens, T., 2004. Evidence-based pharmacotherapy for attention-deficit hyperactivity disorder. Int. J. Neuropsychopharmacol. 7, 77-97.
11. Borsini, F., Podhorna, J., Marazziti, D., 2002. Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology (Berl) 163, 121-141.
12. Breslau, N., 1995. Psychiatric comorbidity of smoking and nicotine dependence. Behav. Genet. 25, 95-101.
13. Breuer, M.E., Chan, J.S., Oosting, R.S., Groenink, L., Korte, S.M., Campbell, U., Schreiber, R., Hanania, T., Snoeren, E.M., Waldinger, M., Olivier, B., 2008. The triple monoaminergic reuptake inhibitor DOV 216,303 has antidepressant effects in the rat olfactory bulbectomy model and lacks sexual side effects. Eur. Neuropsychopharmacol. 18, 908-916.
14. Briggs, C.A., Grønlien, J.H., Curzon, P., Timmermann, D.B., Ween, H., Thorin-Hagene, K., Kerr, P., Anderson, D.J., Malysz, J., Dyhring, T., Olsen, G.M., Peters, D., Bunnelle, W.H., Gopalakrishnan, M., 2009. Role of channel activation in cognitive enhancement mediated by alpha7 nicotinic acetylcholine receptors. Br. J. Pharmacol. 158, 1486-1494.
15. Busch, B., Biederman, J., Cohen, L.G., Sayer, J.M., Monuteaux, M.C., Mick, E., Zallen, B., Faraone, S.V., 2002. Correlates of ADHD among children in pediatric and psychiatric clinics. Psychiatr. Serv. 53, 1103-1111.
16. Castaneda, A.E., Tuulio-Henriksson, A., Marttunen, M., Suvisaari, J., Lonnqvist, J., 2008. A review on cognitive impairments in depressive and anxiety disorders with a focus on young adults. J. Affect Disord. 106, 1-27.
17. Castner, S.A., Smagin, G.N., Piser, T.M., Wang, Y., Smith, J.S., Christian, E.P., Mrzljak, L., Williams, G.V., 2011. Immediate and sustained improvements in working memory after selective stimulation of α7 nicotinic acetylcholine receptors. Biol. Psychiatry 69, 12-18.
18. Chen, Z., Skolnick, P., 2007. Triple uptake inhibitors: therapeutic potential in depression and beyond. Expert Opin. Investig. Drugs 16, 1365-1377.
19. Cheng, Y., Prusoff, W.H., 1973. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 percent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108.
20. Cincotta, S.L., Yorek, M.S., Moschak, T.M., Lewis, S.R., Rodefer, J.S., 2008. Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction. Curr. Opin. Investig. Drugs 9, 47-56.
21. Clark, R.A., Shoaib, M., Hewitt, K.N., Stanford, S.C., Bate, S.T., 2012. A comparison of InVivoStat with other statistical software packages for analysis of data generated from animal experiments. J. Psychopharmacol. 26, 1136-1142.
22. Fox, G.B., Pan, J.B., Esbenshade, T.A., Bennani, Y.L., Black, L.A., Faghih, R., Hancock, A.A., Decker, M.W., 2002. Effects of histamine H(3) receptor ligands GT-2331 and ciproxifan in a repeated acquisition avoidance response in the spontaneously hypertensive rat pup. Behav. Brain Res. 131, 151-161.
23. Fryer, J.D., Lukas, R.J., 1999. Antidepressants noncompetitively inhibit nicotinic acetylcholine receptor function. J. Neurochem. 72, 1117-1124.
24. Gammon, G.D., Brown, T.E., 1993. Fluoxetine and methylphenidate in combination for treatment of attention deficit disorder and comorbid depressive disorder. J. Child Adolesc. Psychopharmacol. 3, 1-10.
25. Gehricke, J.G., Hong, N., Whalen, C.K., Steinhoff, K., Wigal, T.L., 2009. Effects of transdermal nicotine on symptoms, moods, and cardiovascular activity in the everyday lives of smokers and nonsmokers with attention-deficit/ hyperactivity disorder. Psychol. Addict. Behav. 23, 644-655.
26. Gehricke, J.G., Loughlin, S.E., Whalen, C.K., Potkin, S.G., Fallon, J.H., Jamner, L.D., Belluzzi, J.D., Leslie, F.M., 2007. Smoking to self-medicate attentional and emotional dysfunctions. Nicotine Tob. Res. 9 (Suppl. 4), S523-S536.
27. Guiard, B.P., El Mansari, M., Blier, P., 2009. Prospect of a dopamine contribution in the next generation of antidepressant drugs: the triple reuptake inhibitors. Curr. Drug Targets 10, 1069-1084.
28. Hascoet, M., Bourin, M., Colombel, M.C., Fiocco, A.J., Baker, G.B., 2000. Anxiolytic-like effects of antidepressants after acute administration in a four-plate test in mice. Pharmacol. Biochem. Behav. 65, 339-344. http://invivostat.co.uk/.
29. Jørgensen, S., Nielsen, E.O., Peters, D., Dyhring, T., 2008. Validation of a fluorescence-based high-throughput assay for the measurement of neurotransmitter transporter uptake activity. J. Neurosci. Methods 169, 168-176.
30. Kessler, R.C., Adler, L., Barkley, R., Biederman, J., Conners, C.K., Demler, O., Faraone, S.V., Greenhill, L.L., Howes, M.J., Secnik, K., Spencer, T., Ustun, T.B., Walters, E.E., Zaslavsky, A.M., 2006. The prevalence and correlates of adult ADHD in the United States: results from the National Comorbidity Survey Replication. Am. J. Psychiatry 163, 716-723.
31. Kunwar, A., Dewan, M., Faraone, S.V., 2007. Treating common psychiatric disorders associated with attention-deficit/hyperactivity disorder. Expert Opin. Pharmacother. 8, 555-562.
32. Lambert, N.M., Hartsough, C.S., 1998. Prospective study of tobacco smoking and substance dependencies among samples of ADHD and non-ADHD participants. J. Learn. Disabil. 31, 533-544.
33. Lehr, T., Staab, A., Tillmann, C., Nielsen, E.O., Trommeshauser, D., Schaefer, H.G., Kloft, C., 2008. Contribution of the active metabolite M1 to the pharmacological activity of tesofensine in vivo: a pharmacokineticepharmacodynamic modelling approach. Br. J. Pharmacol. 153, 164-174.
34. Levin, E.D., Conners, C.K., Silva, D., Canu, W., March, J., 2001. Effects of chronic nicotine and methylphenidate in adults with attention deficit/hyperactivity disorder. Exp. Clin. Psychopharmacol. 9, 83-90.
35. Linet, L.S., 1989. Treatment of a refractory depression with a combination of fluoxetine and d-amphetamine. Am. J. Psychiatry 146, 803-804.
36. Lukas, R.J., 1986. Characterization of curaremimetic neurotoxin binding sites on cellular membrane fragments derived from the rat pheochromocytoma PC12. J. Neurochem. 47, 1768-1773.
37. Madras, B.K., Spealman, R.D., Fahey, M.A., Neumeyer, J.L., Saha, J.K., Milius, R.A., 1989. Cocaine receptors labeled by [3H]2 beta-carbomethoxy-3 beta-(4-fluorophenyl)tropane. Mol. Pharmacol. 36, 518-524.
38. Mannie, Z.N., Harmer, C.J., Cowen, P.J., Norbury, R., 2010. A functional magnetic resonance imaging study of verbal working memory in young people at increased familial risk of depression. Biol. Psychiatry 67, 471-477.
39. Marin, M.F., Lord, C., Andrews, J., Juster, R.P., Sindi, S., Arsenault-Lapierre, G., Fiocco, A.J., Lupien, S.J., 2011. Chronic stress, cognitive functioning and mental health. Neurobiol. Learn. Mem. 96, 583-595.
40. Masand, P.S., Anand, V.S., Tanquary, J.F., 1998. Psychostimulant augmentation of second generation antidepressants: a case series. Depress. Anxiety 7, 89-91.
41. McClernon, F.J., Hiott, F.B., Westman, E.C., Rose, J.E., Levin, E.D., 2006. Transdermal nicotine attenuates depression symptoms in nonsmokers: a double-blind, placebo-controlled trial. Psychopharmacology (Berl) 189, 125-133.
42. McClintock, S.M., Husain, M.M., Greer, T.L., Cullum, C.M., 2010. Association between depression severity and neurocognitive function in major depressive disorder: a review and synthesis. Neuropsychology 24, 9-34.
43. Millan, M.J., Agid, Y., Brune, M., Bullmore, E.T., Carter, C.S., Clayton, N.S., Connor, R., Davis, S., Deakin, B., DeRubeis, R.J., Dubois, B., Geyer, M.A., Goodwin, G.M., Gorwood, P., Jay, T.M., Joels, M., Mansuy, I.M., Meyer-Lindenberg, A., Murphy, D., Rolls, E., Saletu, B., Spedding, M., Sweeney, J., Whittington, M., Young, L.J., 2012. Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat. Rev. Drug Discov. 11, 141-168.
44. Mutlu, O., Ulak, G., Celikyurt, I.K., Akar, F.Y., Erden, F., 2011. Effects of citalopram on cognitive performance in passive avoidance, elevated plus-maze and three-panel runway tasks in naïve rats. Chin. J. Physiol. 54, 36-46.
45. Nielsen, S.F., Nielsen, E.O., Olsen, G.M., Liljefors, T., Peters, D., 2000. Novel potent ligands for the central nicotinic acetylcholine receptor: synthesis, receptor binding, and 3D-QSAR analysis. J. Med. Chem. 43, 2217-2226.
46. Orr, K., Taylor, D., 2007. Psychostimulants in the treatment of depression: a review of the evidence. CNS Drugs 21, 239-257.
47. Pary, R., Lewis, S., Matuschka, P.R., Lippmann, S., 2002. Attention-deficit/hyperactivity disorder: an update. South Med. J. 95, 743-749.
48. Pandya, A.A., Yakel, J.L., 2013. Activation of the α7 nicotinic ACh receptor induces anxiogenic effects in rats which is blocked by a 5-HT1a receptor antagonist. Neuropharmacology 70C, 35-42.
49. Peters, D., Olsen, G.M., Nielsen, E.,Ø., 2006. Preparation of Novel Naphthyl Substituted Azabicyclo Derivatives and Their Use as Monoamine Neurotransmitter Re-uptake Inhibitors. PCT Int Appl, 23 pp. WO 2006067090 A1.
50. Philip, N.S., Carpenter, L.L., Tyrka, A.R., Price, L.H., 2010. Nicotinic acetylcholine receptors and depression: a review of the preclinical and clinical literature. Psychopharmacology (Berl) 212, 1-12.
51. Picciotto, M.R., Brunzell, D.H., Caldarone, B.J., 2002. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport 13, 1097-1106.
52. Pietrzak, R.H., Mollica, C.M., Maruff, P., Snyder, P.J., 2006. Cognitive effects of immediate-release methylphenidate in children with attention-deficit/hyperactivity disorder. Neurosci. Biobehav. Rev. 30, 1225-1245.
53. Pimontel, M.A., Culang-Reinlieb, M.E., Morimoto, S.S., Sneed, J.R., 2012. Executive dysfunction and treatment response in late-life depression. Int. J. Geriatr. Psychiatry 27, 893-899.
54. Pizzagalli, D.A., 2011. Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36, 183-206.
55. Pomerleau, O.F., Downey, K.K., Stelson, F.W., Pomerleau, C.S., 1995. Cigarette smoking in adult patients diagnosed with attention deficit hyperactivity disorder. J. Subst. Abuse 7, 373-378.
56. Porsolt, R.D., Bertin, A., Jalfre, M., 1977. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327-336.
57. Potter, A.S., Newhouse, P.A., Bucci, D.J., 2006. Central nicotinic cholinergic systems: a role in the cognitive dysfunction in attention-deficit/ hyperactivity disorder? Behav. Brain Res. 175, 201-211.
58. Prickaerts, J., van Goethem, N.P., Chesworth, R., Shapiro, G., Boess, F.G., Methfessel, C., Reneerkens, O.A., Flood, D.G., Hilt, D., Gawryl, M., Bertrand, S., Bertrand, D., König, G., 2012. EVP-6124, a novel and selective α7 nicotinic acetylcholine receptor partial agonist, improves memory performance by potentiating the acetylcholine response of α7 nicotinic acetylcholine receptors. Neuropharmacology 62, 1099-1110.
59. Prins, J., Westphal, K.G., Korte-Bouws, G.A., Quinton, M.S., Schreiber, R., Olivier, B., Korte, S.M., 2011. The potential and limitations of DOV 216,303 as a triple reuptake inhibitor for the treatment of major depression: a microdialysis study in olfactory bulbectomized rats. Pharmacol. Biochem. Behav. 97, 444-452.
60. Redrobe, J.P., Nielsen, E.O., Christensen, J.K., Peters, D., Timmermann, D.B., Olsen, G.M., 2009. Alpha7 nicotinic acetylcholine receptor activation ameliorates scopolamine-induced behavioural changes in a modified continuous Y-maze task in mice. Eur. J. Pharmacol. 602, 58-65.
61. Rezvani, A.H., Kholdebarin, E., Cauley, M.C., Dawson, E., Levin, E.D., 2009. Attenuation of pharmacologically-induced attentional impairment by methylphenidate in rats. Pharmacol. Biochem. Behav. 92, 141-146.
62. Rosenzweig-Lipson, S., Beyer, C.E., Hughes, Z.A., Khawaja, X., Rajarao, S.J., Malberg, J.E., Rahman, Z., Ring, R.H., Schechter, L.E., 2007. Differentiating anti-depressants of the future: efficacy and safety. Pharmacol. Ther. 113, 134-153.
63. Salin-Pascual, R.J., de la Fuente, J.R., Galicia-Polo, L., Drucker-Colin, R., 1995. Effects of transdermal nicotine on mood and sleep in nonsmoking major depressed patients. Psychopharmacology (Berl) 121, 476-479.
64. Schmidt, M.V., Trumbach, D., Weber, P., Wagner, K., Scharf, S.H., Liebl, C., Datson, N., Namendorf, C., Gerlach, T., Kuhne, C., Uhr, M., Deussing, J.M., Wurst, W., Binder, E.B., Holsboer, F., Muller, M.B., 2010. Individual stress vulnerability is predicted by short-term memory and AMPA receptor subunit ratio in the hippocampus. J. Neurosci. 30, 16949-16958.
65. Seignourel, P.J., Kunik, M.E., Snow, L., Wilson, N., Stanley, M., 2008. Anxiety in dementia: a critical review. Clin. Psychol. Rev. 28, 1071-1082.
66. Spalletta, G., Musicco, M., Padovani, A., Rozzini, L., Perri, R., Fadda, L., Canonico, V., Trequattrini, A., Pettenati, C., Caltagirone, C., Palmer, K., 2010. Neuropsychiatric symptoms and syndromes in a large cohort of newly diagnosed, untreated patients with Alzheimer disease. Am. J. Geriatr. Psychiatry 18, 1026-1035.
67. Stoll, A.L., Pillay, S.S., Diamond, L., Workum, S.B., Cole, J.O., 1996. Methylphenidate augmentation of serotonin selective reuptake inhibitors: a case series. J. Clin. Psychiatry 57, 72-76.
68. Sydserff, S., Sutton, E.J., Song, D., Quirk, M.C., Maciag, C., Li, C., Jonak, G., Gurley, D., Gordon, J.C., Christian, E.P., Doherty, J.J., Hudzik, T., Johnson, E., Mrzljak, L., Piser, T., Smagin, G.N., Wang, Y., Widzowski, D., Smith, J.S., 2009. Selective α7 nicotinic receptor activation by AZD0328 enhances cortical dopamine release and improves learning and attentional processes. Biochem. Pharmacol. 78, 880-888.
69. Tamburella, A., Micale, V., Mazzola, C., Salomone, S., Drago, F., 2012. The selective norepinephrine reuptake inhibitor atomoxetine counteracts behavioral impairments in trimethyltin-intoxicated rats. Eur. J. Pharmacol. 683, 148-154.
70. Thomsen, M.S., Hansen, H.H., Timmerman, D.B., Mikkelsen, J.D., 2010. Cognitive improvement by activation of alpha7 nicotinic acetylcholine receptors: from animal models to human pathophysiology. Curr. Pharm. Des. 16, 323-343.
71. Tian, J.W., Jiang, W.L., Zhong, Y., Meng, Q., Gai, Y., Zhu, H.B., Hou, J., Xing, Y., Li, Y.X., 2011. Preclinical pharmacology of TP1, a novel potent triple reuptake inhibitor with antidepressant properties. Neuroscience 196, 124-130.
72. Timmermann, D.B., Gronlien, J.H., Kohlhaas, K.L., Nielsen, E.O., Dam, E., Jorgensen, T.D., Ahring, P.K., Peters, D., Holst, D., Christensen, J.K., Malysz, J., Briggs, C.A., Gopalakrishnan, M., Olsen, G.M., 2007. An allosteric modulator of the alpha7 nicotinic acetylcholine receptor possessing cognition-enhancing properties in vivo. J. Pharmacol. Exp. Ther. 323, 294-307.
73. Wilens, T.E., Biederman, J., Spencer, T.J., Bostic, J., Prince, J., Monuteaux, M.C., Soriano, J., Fine, C., Abrams, A., Rater, M., Polisner, D., 1999. A pilot controlled clinical trial of ABT-418, a cholinergic agonist, in the treatment of adults with attention deficit hyperactivity disorder. Am. J. Psychiatry 156, 1931-1937.
74. Zangrossi Jr., H., Viana, M.B., Zanoveli, J., Bueno, C., Nogueira, R.L., Graeff, F.G., 2001. Serotonergic regulation of inhibitory avoidance and one-way escape in the rat elevated T-maze. Neurosci. Biobehav Rev. 25, 637-645.
75. Zisook, S., Rush, A.J., Haight, B.R., Clines, D.C., Rockett, C.B., 2006. Use of bupropion in combination with serotonin reuptake inhibitors. Biol. Psychiatry 59, 203-210.